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Ann Thorac Surg 2003;75:372-377
© 2003 The Society of Thoracic Surgeons

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Original article: general thoracic

Clinical outcome after coronary artery revascularization and lung transplantation

^a Department of Surgery, Duke University Medical Center, Durham, North Carolina, USA
^b department of Pulmonary Medicine, Duke University Medical Center, Durham, North Carolina, USA

* Address reprint requests to Dr Davis, Duke University Medical Center, Box 3864, Durham, NC 27710, USA.
e-mail: davis053{at}mc.duke.edu

Presented at the Forty-eighth Annual Meeting of the Southern Thoracic Surgical Association, San Antonio, TX, Nov 8–10, 2001.

	Abstract

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
BACKGROUND: Presence of coronary artery disease (CAD) in otherwise eligible lung transplant candidates is considered a contraindication to lung transplantation. We reviewed the clinical outcome of our experience in lung transplant recipients with operable coronary artery disease and normal left ventricular function.

METHODS: Medical records of all transplant recipients with coronary artery disease were reviewed. Data analyzed include demographics, coronary angiograms, coronary artery revascularization procedure, and clinical outcome after lung transplantation.

RESULTS: Between April 1992 and August 2001, 354 lung transplant procedures were performed. Eighteen patients (5%) had significant CAD (greater than 50% stenoses). Six male patients (mean age 59 years) underwent percutaneous transluminal coronary angioplasty/stent and after lung transplantation all were discharged after a median hospital stay of 8.5 days. All recipients are alive at a median follow-up time of 14.5 months after their transplant. Twelve male patients (mean age 58 years) had combined coronary artery bypass grafting and lung transplantation. All recipients were discharged after a median hospital stay of 16 days. Nine recipients are alive at a median follow-up time of 7.5 months after transplant. One-year survival by the Kaplan-Meier method is 88% for the 18 patients with coronary artery disease who underwent revascularization and lung transplantation.

CONCLUSIONS: Despite the traditional criteria of excluding all eligible transplant candidates due to coronary artery disease, coronary revascularization in select candidates with favorable anatomy and normal left ventricular function can allow patients to undergo lung transplantation with acceptable outcomes.

	Introduction

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Since the early days of clinical lung transplantation significant improvements in the immunosuppressive regimens, operative techniques, and patient management after transplantation have allowed an even larger group of patients to benefit from this treatment option [1,2]. The widespread acceptance of organ transplantation as a viable therapeutic alternative combined with improved clinical outcomes and quality of life for the majority of lung transplant recipients have prompted an increased enrollment of eligible candidates onto the United Network for Organ Sharing patient waiting list for lung transplant [3, 4]. Naturally the waiting time to transplantation and patient mortality while waiting for lung transplantation have simultaneously increased. In an effort to keep pace with this growing demand there was a corresponding increase in the number of lung transplants performed since the early 1990s. However, over the last 4 years the number of lung transplants performed has plateaued despite aggressive efforts to increase the supply of donor organs nationwide [5].Partly because of this imbalance between demand and donor organ availability selection criteria for eligible transplant candidates have remained stringent in an effort to maximize favorable patient outcomes after lung transplantation [6].

Presence of significant coronary artery disease and left ventricular dysfunction has traditionally been considered a contraindication to lung transplantation for patients who would otherwise be considered eligible candidates [6, 7]. In the nontransplant population we have seen an increasing body of evidence supporting improvement in quality of life and long-term survival for patients who have had coronary artery revascularization for significant coronary artery disease. This is particularly convincing for patients with normal left ventricular function and complete coronary artery revascularization despite the presence of multivessel disease [8, 9]. We hypothesized that lung transplant candidates with no other disqualifying comorbidities except significant coronary artery disease, favorable coronary anatomy, and preserved left ventricular function should have acceptable clinical outcomes after revascularization and lung transplantation. We reviewed our experience with coronary artery revascularization in lung transplant recipients meeting these criteria.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
Study population
A retrospective review of medical records of all lung transplant patients was conducted and all recipients who underwent coronary angiography during their initial preoperative evaluation were identified. At our center candidates referred for coronary angiography include male patients more than 40 years old, female patients more than 45 years old, and younger patients with cardiac symptoms or significant risk factors. The study population primarily included all lung transplant recipients with presence of significant coronary artery disease who underwent coronary revascularization and transplantation. The data analyzed included demographics (age, sex, etiology of pulmonary disease, and FEV1), cardiac risk factors (gender, hypertension, hypercholesterolemia, diabetes, smoking history, family history, and angina or myocardial infarction), coronary angiograms (coronary artery anatomy, severity of coronary artery disease, left ventricular ejection fraction, and left ventricular wall motion). Coronary artery revascularization procedures and complications, lung transplantation procedures, and posttransplant outcomes (cardiac morbidity/mortality, hospital stay, and survival) were also reviewed. All transplant recipients excluding those who underwent coronary intervention (percutaneous transluminal angioplasty [PTCA]/stent and coronary artery bypass graft [CABG] recipients) refers to the nonrevascularized patient cohort. Given the increased risks associated with the combined therapy, coronary artery revascularization and lung transplant procedures, all eligible candidates offered this alternative were extensively counseled regarding the proposed interventions, the potential risks and complications, and benefits of improving and extending their quality of life. All eligible recipients provided informed consent.

Coronary revascularization procedures
Coronary artery revascularization using PTCA/stent (PTCA/stent group) was performed prior to the lung transplant procedure in selected patients. Percutaneous intervention was pursued after mutual agreement between the intervention cardiology and the transplant team. Patients selected for percutaneous intervention had angiographic findings comparable with those of the low-risk group defined in the anatomic lesion classification system published in the ACC/AHA guidelines for percutaneous coronary intervention [10]. These lesions are readily accessible, discrete, typically concentric, nonostial, and do not involve major side branches. In addition to these favorable anatomic characteristics, all patients were free of known clinical factors other than the use of systemic corticosteroids likely to increase the risk of adverse outcomes and potentially offset prolonged benefit of percutaneous intervention therapy before and after lung transplantation.

The remaining patients (CABG group) underwent surgical revascularization at the time of their lung transplant procedure. Selection of these candidates was also dependent on the anatomic characteristics of their coronary artery disease and the global coronary artery morphology. All recipients had proximal disease despite the presence of additional features such as irregular contours, ostial lesions, and disease involving other major branches. Additionally, another important selection criteria was the presence of adequate distal vessels estimated to be more than 1.5 mm in diameter and the absence of diffuse coronary artery disease despite adequate vessel size. For recipients requiring surgical revascularization, our preferred operative approach is to avoid the use of cardiopulmonary bypass support for both coronary artery revascularization and the lung implantation procedures unless preoperative recipient characteristics or intraoperative events dictate otherwise. Early in our experience, the first 3 patients had the combined procedures planned and performed with the use of cardiopulmonary bypass support. Recently, 2 additional patients who demonstrated significant hemodynamic and ventilatory compromise soon after induction underwent both operative procedures with cardiopulmonary bypass support.

Operative approach
Based on the preoperative assessment, all lung transplant patients are listed for either bilateral, right, or left lung transplant. However, our current preference is bilateral rather than single lung transplantation whenever possible. This is also true for patients who also require concomitant surgical coronary artery revascularization. If bilateral lung donor allograft is not available and a single lung transplant becomes a necessary option, the choice between a right or left single lung transplant is partly determined by the concomitant coronary artery vessel(s) that needed to be grafted.

The preferred approach for the bilateral sequential lung transplant procedure is the bilateral anterolateral thoracosternotomy or the "clamshell" incision [11, 12]. This provides adequate exposure to facilitate the coronary artery revascularization procedure, which is routinely performed first, with or without cardiopulmonary bypass, followed immediately by the lung transplantation procedure. Single lung transplant procedures were performed in 4 patients. Two patients had single right lung transplant and single vessel (right coronary artery) bypass grafting on cardiopulmonary bypass support through a right thoracotomy approach. One patient, using the left posterolateral thoracotomy approach, underwent a single left lung transplant procedure preceded by single vessel (left internal mammary artery to left anterior descending) coronary artery bypass grafting off-pump. One patient underwent three-vessel coronary artery bypass grafting and single right lung transplant procedure with cardiopulmonary bypass support through a median sternotomy extended anterolaterally onto the right chest for the latter procedure. The choice of bypass conduit is the left internal mammary artery for the left anterior descending and saphenous vein grafts for the remaining vessels. The postoperative management has been described previously and all patients are maintained on a triple-drug immunosuppressive regimen [1]. In addition the revascularized patients are also given aspirin and anticholesterol medications long term.

Statistics
Results are presented as mean value ± standard deviation or median value ± standard error for continuous variables. Actuarial survival was determined using the Kaplan-Meier analysis and log-rank analysis for statistical significance. An unpaired Student’s t test was used to compare risk factors for coronary artery disease between the PTCA/stent and CABG groups, and the hospital length of stay for the PTCA/stent, CABG, and nonrevascularized groups.

	Results

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
Study population
Between April 1992 and August 2001, 354 lung transplant procedures were performed at our center. In all 256 patients with a mean age of 57 ± 9 years (range 38 to 67), had coronary angiography performed during their pretransplant assessment. Of these, 100 (39%) patients with a mean age of 63 ± 7 years (range 44 to 66) were identified with presence of coronary artery disease on their coronary angiograms; 82 patients (32%) had nonobstructive coronary artery disease (narrowing < 50%) and 18 patients (7%) were found to have significant coronary artery stenoses (75% or higher).

Of the 18 patients, 6 patients underwent percutaneous transluminal angioplasty/stent before their lung transplant procedure and 12 patients had combined coronary artery bypass grafting (CABG) in conjunction with their lung transplant procedure. All 6 patients within the PTCA/stent group were male. Mean age was 59 ± 5 years (range 49 to 64 years). Chronic obstructive pulmonary disease was the cause of end-stage lung disease in 5 patients and idiopathic pulmonary fibrosis in one patient. In the CABG group, all 12 patients were male with a mean age of 61 ± 8 years (range 38 to 64 years); 7 had chronic obstructive pulmonary disease and 5 had idiopathic pulmonary fibrosis as the cause of end-stage lung disease. The mean percent predicted FEV1 for the chronic obstructive pulmonary disease group and the idiopathic pulmonary disease group was 15% ± 3% and 50% ± 10%, respectively. Based on the clinical history the mean number of risk factors for coronary artery disease were similar for the PTCA/stent and CABG groups, 3.3 ± 1.1 versus 2.7 ± 1.6, respectively (p = 0.2).

Preoperative coronary angiogram findings and coronary revascularization
In the PTCA/stent group 5 patients had intervention for significant coronary artery disease involving 1 vessel and 1 patient had 3 vessels without procedural complications; left ventriculogram revealed normal size and function of the left ventricle with mean ejection fraction of 62% ± 3%.

For patients within the CABG group 17 coronary artery bypass grafts were performed, 9 patients with 1 vessel, 1 patient with 2 vessels, and 2 patients with 3 vessels; all had normal left ventricular wall motion and a mean ejection fraction of 61% ± 8%. Off-pump coronary artery bypass was performed in 7 patients followed immediately by the lung allograft implant and 5 patients had cardiopulmonary bypass support for both coronary artery bypass grafting and lung transplantation. For the latter patients, the mean aortic cross-clamp time was 42 ± 21 minutes to perform the coronary artery revascularization procedure followed by resumption of cardiac electromechanical activity and lung transplantation while still on full cardiopulmonary bypass support. The mean cardiopulmonary bypass support time was 191 ± 76 minutes. No intraoperative cardiac complications were encountered for the entire cohort of CABG patients.

Lung transplant procedure
Single versus bilateral lung transplants was equally distributed within the PTCA/stent group. In the CABG group, 4 patients had single and 8 patients had bilateral lung transplants (1:2). In the nonrevascularized group the proportion of single and bilateral lung transplants performed was similar (2:3). Despite the addition of another operative procedure for the CABG group the total mean operative time for this group was comparable with that of the nonrevascularized group, 310 ± 78 minutes versus 315 ± 77 minutes, respectively. After an appropriate donor allograft is identified for a patient and donor on-site evaluation is acceptable the recipient transplant operation proceeds promptly such that there is usually some redundant time between completion of the recipient hilar dissection for pneumonectomy and arrival of the donor lungs in the operating room. This redundant time, which would normally add to the total operative time for a routine recipient transplant operation, is utilized to perform bypass grafting in recipients who need the combined procedures without significantly lengthening the total operative time.

Clinical outcome
There was no evidence of relevant ischemic abnormalities by postoperative electrocardiography in either the PTCA/stent or CABG patients. Cardiac morbidity for both groups included development of atrial fibrillation with rapid ventricular response in 3 patients in the PTCA/stent group and 7 patients in the CABG group. All 10 patients successfully responded to conventional treatment for their atrial fibrillation events and were discharged in normal sinus rhythm. No patients suffered other complications including pericarditis, mediastinitis, deep chest wall infections, or permanent neurologic dysfunction.

Two patients in the CABG group required reexploration for postoperative bleeding. One patient was found to have persistent oozing from the subcarinal lymph node bed and had an uneventful subsequent recovery. The second patient developed delayed cardiac tamponade on the second postoperative day while on percutaneous venovenous extracorporeal membrane oxygenator support for primary graft failure after an oxygenator circuit change. At the time of operative reexploration no surgical bleeding was found.

Four patients within the CABG group had prolonged ventilator dependency. Two of these patients were extubated in the immediate perioperative period. One patient was reintubated at 4 weeks for progressive dyspnea due to bacterial pneumonia in addition to preexisting ischemia reperfusion lung injury; in the second patient reintubation was required owing to respiratory failure associated with respiratory syncytial virus pneumonia. These 2 patients were supported for 2 and 4 weeks, respectively. The third patient required extracorporeal oxygenator support and retransplant for primary graft failure. His postoperative course was also complicated by generalized myopathy and inability to mobilize his pulmonary secretions necessitating slow progressive ventilator wean and repeat daily bronchoscopy for pulmonary hygiene for 6 weeks. The fourth patient failed repeated attempts to extubate in the perioperative period owing to poor mechanics; adenoviral pneumonia complicated his subsequent overall clinical course.

The median hospital length of stay was longer for the CABG group compared with the PTCA/stent group, 16 ± 9.5 days versus 9 ± 0.7 days, respectively (p = 0.01). In comparison, the median hospital length of stay for the nonrevascularized group was 13 ± 1.8 days (p = not significant between groups). All 6 patients in the PTCA/stent cohort are alive with a median follow-up time of 14.5 ± 4.4 months (range 12 to 40). Within the CABG group, 9 patients are alive with a median follow-up time of 8 ± 5.1 months (range 3 to 56). One patient died 56 months after lung transplant of chronic rejection and was free of any cardiac events during the follow-up period. Two patients died 3 months after their lung transplant procedure of complications secondary to adenoviral and respiratory syncytial virus pneumonia. Both patients had normal echocardiographic studies performed before their death. The 1-year survival for the revascularized group (all 18 patients) and the nonrevascularized patient cohort (n = 219) is 88% and 81%, respectively (p value 0.34). For comparison, the latter group included all patients since 1997, the time period during which most recipients underwent coronary intervention. The survival curves are depicted in Figure 1.

View larger version (15K): [in this window] [in a new window]   Fig 1. Kaplan-Meier survival curves for lung transplant recipients with coronary revascularization (n = 18) and the nonrevascularized recipient cohort (n = 219). Solid line = controls; dashed line = coronary artery bypass graft/percutaneous transluminal coronary angioplasty (CABG/PTCA); open circles = controls, censored; solid circles = CABG/PTCA, censored.

	Comment

Top Abstract Introduction Patients and methods Results Comment Discussion References

Thaik and associates [19] reported their findings from a pool of potential lung transplant candidates who underwent coronary angiography based on cardiac risk stratification. Substantial coronary artery disease was found in only 6% of all those who underwent angiography before listing and the majority of them had more than five cardiac risk factors. It appears that the presence of clinically significant coronary artery disease in candidates referred for transplant evaluation is low and more likely to occur in those with significant cardiac risk factors. Its absence or clinical relevance if suspected cannot reliably be dismissed based on the currently available noninvasive methods. At present, coronary angiography is the procedure of choice to evaluate the presence of coronary artery disease and possibly offer an opportunity to identify patients who may be eligible for coronary artery revascularization and lung transplantation.

Coronary artery revascularization has been described in a few lung transplant recipients [17, 19, 20]. Snell and colleagues [17] reported their experience in 5 patients: 2 patients underwent PTCA/stent before their transplant procedure (both were alive after discharge) and 3 patients had coronary artery bypass grafting combined with their transplant procedure (2 died 75 days and 255 days after the procedure of acute rejection and cytomegalovirus infection, respectively). In our series no deaths were due to cardiac events. Atrial fibrillation was the most frequent cause of minor cardiac morbidity postoperative. This complication has also been previously reported [15, 16]. These patients have a higher propensity for such events given their underlying cardiac disease, end-stage pulmonary disease, older age, and operative intervention [21–23]. All patients were successfully managed with conventional treatment [24] and remained in normal sinus at the time of discharge and clinic follow-up. All patients during their perioperative and follow-up period remained free of any other adverse cardiac events. The postoperative complications including reexploration for bleeding, primary graft failure, pneumonia, and prolonged ventilator support are recognized adverse events after lung transplantation. In the CABG group, 4 of 12 patients required a tracheostomy and we acknowledge this is atypical. As previously noted all 4 patients had unique clinical events dictating the need for a tracheostomy and these events may have contributed to similar results in the nonrevascularized transplant patients. The addition of coronary intervention did not adversely change the operative time or length of hospital stay for the study group compared with the nonrevascularized patient cohort. Patients in the PTCA/stent group had shorter time to discharge compared with the CABG group but not significantly different from that of the nonrevascularized group.

The limitations of this study are that it is a retrospective study with a small sample size, limited long-term follow-up, and obviously, given the unique patient population and limited number of coronary interventions, long-term graft patency for both the PTCA/stent and CABG groups remains unknown. In a retrospective analysis with nonsimultaneous application of the PTCA/stent and transplant procedures, it is also quite possible to underestimate the morbidity and mortality if these patients are not carefully followed up or die while waiting for transplantation. In our series no patients suffered any morbidity or mortality before or after their PTCA/stent procedure and all were successfully transplanted. Despite the advances in coronary intervention technology [25] and proven long-term survival after coronary bypass grafting in the nontransplant population, favorable long-term outcomes in the lung transplant recipients with coronary artery revascularization cannot be inferred until proven otherwise.

In conclusion a careful preoperative assessment of coronary artery anatomy and ventricular function in lung transplant candidates lowers the operative risk and help defines a subset of patients with significant coronary artery disease who might benefit from coronary intervention and lung transplant. Discrete large vessel disease and preserved left ventricular function as noted in our series may allow for safe intervention with PTCA/stent in carefully selected patients before lung transplant and combined CABG and lung transplant in the remaining candidates. Cardiac morbidity and hospital length of stay appear to be acceptable.

	Discussion

Top Abstract Introduction Patients and methods Results Comment Discussion References

 
DR THORALF SUNDT (Rochester, MN): As surgeons, we are very good at talking about what we can do. What is tougher is talking about what we should do. You opened your discussion with a review of the critical mismatch in numbers of donors and recipients. Now are you suggesting that we broaden our inclusion criteria? You have demonstrated that you can combine coronary revascularization and lung transplantation. Should you?

DR PATEL: You are absolutely correct in highlighting the discrepancy between available donor organs and eligible recipients. I think one of the premises of this paper is to show that we are not advocating liberalizing the criteria for all potential lung transplant candidates who also have coronary artery disease. There is a subset of patients among this group to whom we can selectively offer this therapy with acceptable outcomes. I would emphasize that these patients have undergone the rigorous pretransplant screening process and have, besides their end-stage lung disease, discrete coronary artery lesions with favorable anatomy for revascularization, normal left ventricular function, and no other comorbidities. Adhering to these criteria would limit eligible candidates and offer this therapy to patients who would otherwise be denied lung transplantation.

DR W. STEVES RING (Dallas, TX): Coronary artery disease frequently is a marker of peripheral vascular disease and cerebrovascular disease. How are you screening those patients out? Secondly, which patients with coronary artery disease and normal ventricular function would you currently turn down for transplantation?

DR PATEL: To answer your first question, the indication to evaluate for, for example, carotid artery disease would be based on clinical history and physical findings. We do not routinely have all patients undergo vascular evaluation. To answer your second question, if they have normal left ventricular function, what we are emphasizing is that the coronary artery lesions have to be quite discrete and the coronary artery anatomy favorable for therapeutic intervention. There is always going to be progression of the disease. We would not recommend patients with depressed ventricular function, patients with diffuse atherosclerosis and small vessels despite normal function, and patients with significant other comorbidities.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Vijay S. Patel Robert H. Messier Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Patel, V. S. Articles by Davis, R.D. Search for Related Content PubMed PubMed Citation Articles by Patel, V. S. Articles by Davis, R.D. Related Collections Lung - transplantation